Letter | Published:

Unidirectional pulmonary airflow patterns in the savannah monitor lizard

Nature volume 506, pages 367370 (20 February 2014) | Download Citation

Abstract

The unidirectional airflow patterns in the lungs of birds have long been considered a unique and specialized trait associated with the oxygen demands of flying, their endothermic metabolism1 and unusual pulmonary architecture2,3. However, the discovery of similar flow patterns in the lungs of crocodilians indicates that this character is probably ancestral for all archosaurs—the group that includes extant birds and crocodilians as well as their extinct relatives, such as pterosaurs and dinosaurs4,5,6. Unidirectional flow in birds results from aerodynamic valves, rather than from sphincters or other physical mechanisms7,8, and similar aerodynamic valves seem to be present in crocodilians4,5,6. The anatomical and developmental similarities in the primary and secondary bronchi of birds and crocodilians suggest that these structures and airflow patterns may be homologous4,5,6,9. The origin of this pattern is at least as old as the split between crocodilians and birds, which occurred in the Triassic period10. Alternatively, this pattern of flow may be even older; this hypothesis can be tested by investigating patterns of airflow in members of the outgroup to birds and crocodilians, the Lepidosauromorpha (tuatara, lizards and snakes). Here we demonstrate region-specific unidirectional airflow in the lungs of the savannah monitor lizard (Varanus exanthematicus). The presence of unidirectional flow in the lungs of V. exanthematicus thus gives rise to two possible evolutionary scenarios: either unidirectional airflow evolved independently in archosaurs and monitor lizards, or these flow patterns are homologous in archosaurs and V. exanthematicus, having evolved only once in ancestral diapsids (the clade encompassing snakes, lizards, crocodilians and birds). If unidirectional airflow is plesiomorphic for Diapsida, this respiratory character can be reconstructed for extinct diapsids, and evolved in a small ectothermic tetrapod during the Palaeozoic era at least a hundred million years before the origin of birds.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone. Biol. Rev. Cambr. Phil. Soc. 81, 545–579 (2006)

  2. 2.

    Lung-air-sac anatomy and respiratory pressures in the bird. J. Exp. Biol. 57, 543–550 (1972)

  3. 3.

    Spectacularly robust! Tensegrity principle explains the mechanical strength of the avian lung. Respir. Physiol. Neurobiol. 155, 1–10 (2007)

  4. 4.

    The provenance of alveolar and parabronchial lungs: insights from paleoecology and the discovery of cardiogenic, unidirectional airflow in the American alligator (Alligator mississippiensis). Physiol. Biochem. Zool. 83, 561–575 (2010)

  5. 5.

    & Unidirectional airflow in the lungs of alligators. Science 327, 338–340 (2010)

  6. 6.

    , & Pulmonary anatomy in the Nile crocodile and the evolution of unidirectional airflow in Archosauria. PeerJ (2013)

  7. 7.

    , & Inspiratory valving in avian bronchi: aerodynamic considerations. Respir. Physiol. 72, 241–255 (1988)

  8. 8.

    Structure and function of the lung of birds. Poult. Sci. 30, 3–10 (1951)

  9. 9.

    & The pulmonary anatomy of Alligator mississippiensis and its similarity to the avian respiratory system. Anat. Rec. 295, 699–714 (2012)

  10. 10.

    The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Mus. Nat. Hist. 352, 1–292 (2011)

  11. 11.

    in Biology of the Reptilia Vol. 19 (Morphology G) (eds & ) 1–92 (Society for the Study of Amphibians and Reptiles, 1998)

  12. 12.

    , & Earliest example of a giant monitor lizard (Varanus, Varanidae, Squamata). PLoS ONE 7, e41767 (2012)

  13. 13.

    , , , & Oldest known Varanus (Squamata: Varanidae) from the Upper Eocene and Lower Oligocene of Egypt: support for an African origin of the genus. Palaeontology 53, 1099–1110 (2010)

  14. 14.

    , & Evolution of extreme body size disparity in monitor lizards (Varanus). Evolution 65, 2664–2680 (2011)

  15. 15.

    Evolution of body size: varanid lizards as a model system. Am. Nat. 146, 398–414 (1995)

  16. 16.

    & Standard and maximal metabolic rates of goannas (Squamata: Varanidae). Physiol. Zool. 70, 307–323 (1997)

  17. 17.

    , , & Contribution of the gular pump to ventilation. Science 284, 1661–1663 (1999)

  18. 18.

    , & Die Lungenmorphologie der Warane (Reptilia: Varanidae) und ihre systematisch-stammesgeschichtliche Bedeutung. Bonn. Zool. Beitr. 40, 27–56 (1989)

  19. 19.

    , & The postpulmonary septum of Varanus salvator and its implication for Mosasaurian ventilation and physiology. Bull. Soc. Geol. Fr. 183, 159–169 (2012)

  20. 20.

    Eine Bauplananalyse der Waranlunge. Zool. Beitr. Neue Folge 16, 401–440 (1970)

  21. 21.

    , , , & Scanning electron microscope study of the morphology of the reptilian lung: the savanna monitor lizard Varanus exanthematicus and the Pancake Tortoise Malacochersus tornieri. Anat. Rec. 224, 514–522 (1989)

  22. 22.

    & Lung architecture, volume and static mechanics in five species of lizards. Respir. Physiol. 34, 61–81 (1978)

  23. 23.

    in Biology of the Reptilia Vol. 19 (Morphology G) (eds & ) 93–295 (Society for the Study of Amphibians and Reptiles, 1998)

  24. 24.

    Beiträge zur Kenntniss der Reptilienlunge. Zool. Jahrb. 7, 545–592 (1894)

  25. 25.

    Beiträge zur Kenntnis der Reptilienlunge. II. Zool. Jahrb. 10, 93–156 (1897)

  26. 26.

    & Pulmonary mechanics and the work of breathing in the lizard, Gekko gecko. J. Exp. Biol. 113, 187–202 (1984)

Download references

Acknowledgements

We thank J. Dix (Reptile Rescue Service) for the donation of deceased varanid specimens, J. Bourke for assistance with Avizo, and D. Shafer for German translations. This work was supported by an American Association of Anatomists Postdoctoral Fellowship and an American Philosophical Society Franklin Research Grant to E.R.S., National Science Foundation grants to C.G.F. (IOS-1055080 and IOS-0818973) and a generous donation to the Farmer laboratory by S. Meyer.

Author information

Affiliations

  1. Department of Biology, University of Utah, Salt Lake City, Utah 84112, USA

    • Emma R. Schachner
    • , Robert L. Cieri
    •  & C. G. Farmer
  2. Division of Sleep Medicine, Department of Medicine, Harvard Medical School, Boston, Massachusetts 02215, USA

    • James P. Butler
  3. Molecular and Integrative Physiologic Science Program, Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts 02115, USA

    • James P. Butler

Authors

  1. Search for Emma R. Schachner in:

  2. Search for Robert L. Cieri in:

  3. Search for James P. Butler in:

  4. Search for C. G. Farmer in:

Contributions

E.R.S. and R.L.C. conducted the in vivo surgeries. All authors collected data on excised lungs. E.R.S. acquired the CT scans and generated the three-dimensional digital models. C.G.F. and J.P.B. supervised and contributed ideas throughout the project. All authors contributed to the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Emma R. Schachner or C. G. Farmer.

Supplementary information

Videos

  1. 1.

    3D model of the skeletal and pulmonary anatomy of Varanus exanthematicus

    A volume rendered three dimensional skeleton and segmented surface of the lungs and bronchial tree (left craniolateral view) of a female Varanus exanthematicus generated from a CT scan. The bronchus in which in vivo unidirectional flow was measured is indicated. Abbreviations: cb, cervical bronchus; L1-L10, lateral bronchi 1-10; M1-M11, medial bronchi 1-11.

  2. 2.

    Unidirectional movement of fluid through regions of the lung in V. exanthematicus

    Microsphere infused saline flowing from lateral bronchus 10 to lateral bronchus 9 in an excised right lung during manual ventilation (60 cc syringe). The microspheres can be seen moving from right to left (caudal to cranial) during inspiration and expiration. Abbreviations: L9, lateral bronchus 9; L10, lateral bronchus 10.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature12871

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.